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Substitution of natural sensory input by artificial neurostimulation of an amputated trigeminal nerve does not prevent the degeneration of basal forebrain cholinergic circuits projecting to the somatosensory cortex.

Herrera-Rincon C, Panetsos F - Front Cell Neurosci (2014)

Bottom Line: Stimulation of the cut nerve reverses the metabolic decline but does not affect the decrease in cholinergic fibers in cortex or cholinergic neurons in basal forebrain.MBN ChAT downregulation is not due to a decrease of afferent activity or to a failure of trophic support.Our data support the existence of a modality-specific cortex-MBN-cortex circuit for cognitive information processing.

View Article: PubMed Central - PubMed

Affiliation: Neurocomputing and Neurorobotics Research Group, Universidad Complutense de Madrid Madrid, Spain ; Biomathematics Department, Faculty of Biology and Faculty of Optics, Universidad Complutense de Madrid Madrid, Spain ; Instituto de Investigación Sanitaria del Hospital Clínico San Carlos Madrid, Spain.

ABSTRACT
Peripheral deafferentation downregulates acetylcholine (ACh) synthesis in sensory cortices. However, the responsible neural circuits and processes are not known. We irreversibly transected the rat infraorbital nerve and implanted neuroprosthetic microdevices for proximal stump stimulation, and assessed cytochrome-oxidase and choline- acetyl-transferase (ChAT) in somatosensory, auditory and visual cortices; estimated the number and density of ACh-neurons in the magnocellular basal nucleus (MBN); and localized down-regulated ACh-neurons in basal forebrain using retrograde labeling from deafferented cortices. Here we show that nerve transection, causes down regulation of MBN cholinergic neurons. Stimulation of the cut nerve reverses the metabolic decline but does not affect the decrease in cholinergic fibers in cortex or cholinergic neurons in basal forebrain. Artifical stimulation of the nerve also has no affect of ACh-innervation of other cortices. Cortical ChAT depletion is due to loss of corticopetal MBN ChAT-expressing neurons. MBN ChAT downregulation is not due to a decrease of afferent activity or to a failure of trophic support. Basalocortical ACh circuits are sensory specific, ACh is provided to each sensory cortex "on demand" by dedicated circuits. Our data support the existence of a modality-specific cortex-MBN-cortex circuit for cognitive information processing.

No MeSH data available.


Related in: MedlinePlus

Retrogradely labeled MBN neurons after fluoro-gold (FG) injections in the barrel cortex. Fluorescent micrographs (UV filter) showing cell bodies in MBN that have been retrogradely labeled after bilateral-FG injection in the ipsilateral (non-affected, left) and the contralateral (deafferented, right) barrel cortex. MBN-cortical projecting neurons are diffusely scattered through MBN but they are mainly located in the caudal zone (somatosensory area, red arrow). Deafferentation results in a global neuronal damage being more intense in the specific somatosensory MBN area. In the ipsilateral hemisphere lateral is left; in the contralateral hemisphere lateral is right; rostral is top. Scale bar = 200 μm.
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Figure 6: Retrogradely labeled MBN neurons after fluoro-gold (FG) injections in the barrel cortex. Fluorescent micrographs (UV filter) showing cell bodies in MBN that have been retrogradely labeled after bilateral-FG injection in the ipsilateral (non-affected, left) and the contralateral (deafferented, right) barrel cortex. MBN-cortical projecting neurons are diffusely scattered through MBN but they are mainly located in the caudal zone (somatosensory area, red arrow). Deafferentation results in a global neuronal damage being more intense in the specific somatosensory MBN area. In the ipsilateral hemisphere lateral is left; in the contralateral hemisphere lateral is right; rostral is top. Scale bar = 200 μm.

Mentions: By means of bilateral injections of fluorescent tracers in the barrel cortices of four deafferented additional rats we retrogradely labeled MBN neurons that projected to these barrel cortices. Labeled cells were mainly localized at caudal level in both, left and right MBN (Figure 6). Qualitative morphological analysis, quantitative estimations, and inter-hemispheric comparisons revealed a significantly lower number of retrogradely labeled neurons in the MBN that projected to deafferented somatosensory cortices in all four animals. Loss of corticopetal neurons was observed alongside the whole MBN. However, absence of projecting cells was prominent in the caudal region: interhemispheric differences reached −43 ± 10% in the caudal MBN (P < 0.01) and −17 ± 9% in the rostral (P = 0.06). Caudal zone corresponded to the region with maximum drop of ChAT-positive neurons (Figure 5A).


Substitution of natural sensory input by artificial neurostimulation of an amputated trigeminal nerve does not prevent the degeneration of basal forebrain cholinergic circuits projecting to the somatosensory cortex.

Herrera-Rincon C, Panetsos F - Front Cell Neurosci (2014)

Retrogradely labeled MBN neurons after fluoro-gold (FG) injections in the barrel cortex. Fluorescent micrographs (UV filter) showing cell bodies in MBN that have been retrogradely labeled after bilateral-FG injection in the ipsilateral (non-affected, left) and the contralateral (deafferented, right) barrel cortex. MBN-cortical projecting neurons are diffusely scattered through MBN but they are mainly located in the caudal zone (somatosensory area, red arrow). Deafferentation results in a global neuronal damage being more intense in the specific somatosensory MBN area. In the ipsilateral hemisphere lateral is left; in the contralateral hemisphere lateral is right; rostral is top. Scale bar = 200 μm.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231972&req=5

Figure 6: Retrogradely labeled MBN neurons after fluoro-gold (FG) injections in the barrel cortex. Fluorescent micrographs (UV filter) showing cell bodies in MBN that have been retrogradely labeled after bilateral-FG injection in the ipsilateral (non-affected, left) and the contralateral (deafferented, right) barrel cortex. MBN-cortical projecting neurons are diffusely scattered through MBN but they are mainly located in the caudal zone (somatosensory area, red arrow). Deafferentation results in a global neuronal damage being more intense in the specific somatosensory MBN area. In the ipsilateral hemisphere lateral is left; in the contralateral hemisphere lateral is right; rostral is top. Scale bar = 200 μm.
Mentions: By means of bilateral injections of fluorescent tracers in the barrel cortices of four deafferented additional rats we retrogradely labeled MBN neurons that projected to these barrel cortices. Labeled cells were mainly localized at caudal level in both, left and right MBN (Figure 6). Qualitative morphological analysis, quantitative estimations, and inter-hemispheric comparisons revealed a significantly lower number of retrogradely labeled neurons in the MBN that projected to deafferented somatosensory cortices in all four animals. Loss of corticopetal neurons was observed alongside the whole MBN. However, absence of projecting cells was prominent in the caudal region: interhemispheric differences reached −43 ± 10% in the caudal MBN (P < 0.01) and −17 ± 9% in the rostral (P = 0.06). Caudal zone corresponded to the region with maximum drop of ChAT-positive neurons (Figure 5A).

Bottom Line: Stimulation of the cut nerve reverses the metabolic decline but does not affect the decrease in cholinergic fibers in cortex or cholinergic neurons in basal forebrain.MBN ChAT downregulation is not due to a decrease of afferent activity or to a failure of trophic support.Our data support the existence of a modality-specific cortex-MBN-cortex circuit for cognitive information processing.

View Article: PubMed Central - PubMed

Affiliation: Neurocomputing and Neurorobotics Research Group, Universidad Complutense de Madrid Madrid, Spain ; Biomathematics Department, Faculty of Biology and Faculty of Optics, Universidad Complutense de Madrid Madrid, Spain ; Instituto de Investigación Sanitaria del Hospital Clínico San Carlos Madrid, Spain.

ABSTRACT
Peripheral deafferentation downregulates acetylcholine (ACh) synthesis in sensory cortices. However, the responsible neural circuits and processes are not known. We irreversibly transected the rat infraorbital nerve and implanted neuroprosthetic microdevices for proximal stump stimulation, and assessed cytochrome-oxidase and choline- acetyl-transferase (ChAT) in somatosensory, auditory and visual cortices; estimated the number and density of ACh-neurons in the magnocellular basal nucleus (MBN); and localized down-regulated ACh-neurons in basal forebrain using retrograde labeling from deafferented cortices. Here we show that nerve transection, causes down regulation of MBN cholinergic neurons. Stimulation of the cut nerve reverses the metabolic decline but does not affect the decrease in cholinergic fibers in cortex or cholinergic neurons in basal forebrain. Artifical stimulation of the nerve also has no affect of ACh-innervation of other cortices. Cortical ChAT depletion is due to loss of corticopetal MBN ChAT-expressing neurons. MBN ChAT downregulation is not due to a decrease of afferent activity or to a failure of trophic support. Basalocortical ACh circuits are sensory specific, ACh is provided to each sensory cortex "on demand" by dedicated circuits. Our data support the existence of a modality-specific cortex-MBN-cortex circuit for cognitive information processing.

No MeSH data available.


Related in: MedlinePlus